Abdominal obesity,
considered a risk factor for several morbidities1, consists of two
distinct fat compartments: subcutaneous and visceral fat2. Several
authors have shown that visceral, but not subcutaneous fat, is associated with
several deleterious effects, such as high levels of triglycerides (TG), low
high-density lipoprotein (HDL-C), insulin sensitivity3,4, hyperglycemia,
C4 peptide, metabolic syndrome3-5, endothelial dysfunction6,
hepatic and muscle steatosis, low levels of peptin and adiponectin4,
and smaller and denser low density lipoprotein (LDL)7. Thus, the
accumulation of visceral fat is considered a major risk factor for cardiovascular
(CVD) and metabolic diseases7.

Although the exact
molecular mechanism responsible for this association is unknown, the effect
may occur due to the anatomical location of fat within the abdomen or the differences
in metabolic properties3.

Thus, the reduction
of visceral fat can be a preventive measure for the metabolic syndrome and CVD7.
The measurement of Visceral Adipose Tissue (VAT) has therefore particular implication
on public health8 and the reliability of its measurement is of great
clinical importance9.

Few studies have
determined the prevalence of visceral obesity in different populations10-12,
probably due to the limitations of radiological methods, capable of differentiating
the components of abdominal fat in subcutaneous and visceral fat, in addition
to the inability of anthropometric measurements to represent the VAT area particularly13.
Computed tomography (CT), Magnetic Resonance Imaging (MRI) and ultrasonography
(USG) have high cost, limited availability of equipment and submit the individuals
undergoing assessment to radiation (CT)14,15, preventing their use
for the assessment in large groups of individuals, precluding its use as a screening
tool for the population16.

Therefore, this
study aimed to determine the prevalence of visceral obesity in young women from
the state of Pernambuco, Brazil, based on a predictive equation, and to evaluate
the association of visceral fat with risk factors for CVD.

Methods

The present was
a cross-sectional population-based study, based on data from the ""III Health
and Nutrition State Survey", (PESN III)", held in urban and rural areas of Pernambuco
between May and October 2006.

The present study
involved adult females aged 25 to 36 years of age. To calculate the sample size,
we considered the prevalence of visceral obesity of 28.7%11, an estimation
error of 4% and a confidence level of 95%, totaling 491 individuals. The III
PESN database contained 669 women aged 25 to 36 years; however, of these, 152
were excluded due to lack of clinical data, and thus a total of 517 women who
had all the variables used in this study were enrolled. The III PESN adopted
as exclusion criteria pregnant women and women with physical limitations that
impaired the anthropometric measurements.

Height was measured
using a portable stadiometer (Alturaexata Ltda.) with a precision of 1 mm. The
subjects were positioned upright, barefoot, with upper limbs hanging on the
sides of the body, and heels, back and head touching the wooden column. Weight
was measured using a digital scale (Model MEA-03200/Plenna) with a capacity
of 150 kg and 100-gram scale, with the individual barefoot and wearing light
clothing. To ensure their accuracy, two weight and height measurements were
obtained, and when the difference exceeded 0.5 cm in height and 100 g in weight,
the measurement was repeated and the two closest measurements were written down,
and the mean value was used.

Nutritional status
was classified using weight and height measurements through the Body Mass Index
(BMI), by adopting the cutoffs recommended by the World Health Organization
(WHO), 199817.

Waist Circumference
(WC) was measured in duplicate at the midpoint between the last rib and the
iliac crest, with a tape measure, following the WHO protocol, 199818,
and values > 80 cm were considered high18.

The Waist-to-Height
Ratio (WHtR) was determined by dividing the WC (cm) by the height (cm) and the
cutoff point adopted for discrimination of abdominal obesity and cardiovascular
risk was > 0.5319.

The measurements
of total cholesterol (TC), triglycerides (TG) and fasting glucose (FG) were
measured in venous blood by cubital puncture after a 12-hour overnight fast.
Plasma concentrations of TC and TG were determined by absorption photometry
with enzymatic method. The reference values were those recommended by the III
Brazilian Guidelines on Dyslipidemia20. The FG measurement was performed
using the Accutrend GCT equipment, read immediately after venipuncture, and
the cutoff points adopted were those recommended by the American Diabetics Association,
201021.

The diastolic and
systolic blood pressures (SBP and DBP) were determined using a calibrated aneroid
sphygmomanometer (Premium EC 0483), adopting the protocol and classification
of the VI Brazilian Guidelines on Hypertension (2010)22.

The volume of visceral
fat (VVF) was estimated using the predictive equation proposed by Petribú23
that uses as independent variables the WHtR and FG, as follows:

VVF
= -130.941 + (198.673 x WHtR) + (1.185 x FG);

This equation,
developed from a multiple regression analysis by adopting the USG as a reference
standard, is capable of predicting the VVF in approximately 45%, with a standard
error of estimate of ± 15.19 cm2. The validation was performed
by comparing the VVF measured by the equation and measured by ultrasonography
in a group of women not participating in the stage of development of the equation
using the Student's t test for paired samples, with no statistically
significant difference between the values (54.28 ± 9.79 vs. 53.36
± 7.94, respectively, p = 0.760)23. At an additional step, to
assess the agreement between the two methods, the Bland Altman was carried out
and there was a good agreement, with a bias close to zero (Figure
1). A cutoff of 100 cm2 was adopted for the diagnosis of visceral
obesity24.

The database was
compiled using the Epi Info software release 6.04 (CDC/WHO, Atlanta, GE, USA),
with double entry, and further use of the validation mode to check for any typing
errors. For statistical analyses, we used the SPSS software, release 10.0 (SPSS
Inc., Chicago, IL, USA). Continuous variables were tested according to the normal
distribution using the Kolmogorov-Smirnov test. When they had a non-normal distribution,
they were transformed to their natural logarithm and retested for normality
(age, weight, SBP, DBP, FG, TG, TC, BMI, VVF). When they maintained the non-normal
distribution (age, SBP, DBP, FG, TC), they were described as median and interquartile
range and the non-parametric tests were applied.

The comparison
between the medians was carried out by nonparametric Mann Whitney test. The
association between continuous variables was performed by Spearman's linear
correlation test. The significance level was set at 5% to reject the null hypothesis.

The III PESN research
project was approved by the Research Ethics Committee in Humans of Instituto
de Medicina Integral Professor Fernando Figueira (IMIP), on January 12, 2006
(Protocol No. 709/2006). Women who agreed to participate in the study signed
an informed consent form.

This study was
funded by the National Council for Scientific and Technological Development
(CNPq) (Process No. 505540/2004-5 and 501989/2005-4), being a collaborative
study of the following institutions: Universidade Federal de Pernambuco (UFPE),
IMIP and Health Secretariat of the state of Pernambuco.

Results

The women's median
age was 29 years (CI: 27-32). In general, this was an overweight population
according to BMI, in addition to a high concentration of abdominal fat, as shown
by WC and WHtR. Regarding SBP and DBP, laboratory parameters (FG, TG and TC)
and the VVF estimated by the predictive equation, the values corresponding
to the mean or median were below the reference values (Table
1).

Regarding the nutritional
status, there was a low prevalence of underweight and a high prevalence of overweight
and obesity based on BMI. About 30% of the women had visceral obesity and more
than half, abdominal obesity according to WC and WHtR (Table
2).

About 10% of the
women had SBP and/or DBP alterations. The prevalence of hyperglycemia was close
to 30%, while almost 40% had increased TG. Regarding the TC, only 13% had hypercholesterolemia
(Table 3).

Table
4 shows the comparison between the medians of BMI, SBP, DBP, TG and TC in
women with and without visceral obesity. With the exception of TC, all parameters
were higher in the group with visceral obesity (p <0.002).

The correlations
between SBP, DBP, TG and TC and VVF estimated from the equation are described
in Figure 2.

All variables showed
a positive and significant correlation with VVF, but such correlations were
weak. Moreover, age also showed a significant and positive correlation with
VVF (r = 0.171, p < 0.0001).

Discussion

The population
analyzed in this study was classified as overweight according to their mean
BMI, in addition to showing mean values of WC and WHtR above the cutoff in the
evaluation of abdominal obesity. Nevertheless, they had a mean VVF < 100
cm2. Similar data were observed by Piernas Sánchez et al11,
who applied a predictive equation to a population of 230 women, mean age 39
± 12 years and mean BMI of 29 ± 5 kg/m2, and observed that,
despite being overweight, having high body fat percentage and high cardiovascular
risk according to WC and WHtR, the women had subcutaneous, but not visceral
fat. These authors stressed the fact that women tend to accumulate more subcutaneous
fat in the abdominal region, which could explain these findings11.

Unlike the above,
Onat et al25 found in their study, which also involved women classified
as overweight with abdominal obesity according to the mean BMI and WC, respectively,
a much higher mean of VVF than that of the present study (120.5 ± 58 cm2).
It is noteworthy the fact that the study was conducted in a population with
a mean age of 49 ± 8.7 years with a high prevalence of metabolic syndrome
(34%)25. These authors emphasized the significant increase in VAT
with age and a 42% higher mean in the group with metabolic syndrome25,
which may explain the difference observed when compared with the present study,
which involved younger women, less likely to have metabolic syndrome. In relation
to the increase in the VVF according to age, these results were also described
by Pascot et al26, who found a mean VVF of 63.7 ± 40.9 cm2
in young women (27.4 ± 7.5 years) and 116.1 ± 67.5 cm2
in middle-aged women (49.5 ± 5.3 years), with this difference being statistically
significant. This study also showed a positive correlation between age and VVF.

Literature reports
that the prevalence of abdominal obesity has increased over the last decade
and now exceeds the prevalence of overall obesity, with rates of 61.3% in women27,28.
Such evidence was also found in the present study, which found a prevalence
of 17% of overall obesity and 62.9% of abdominal obesity according to the WC.

The prevalence
of visceral obesity was lower than the abdominal obesity, which was expected,
considering that the WC is more strongly associated with subcutaneous fat than
with visceral fat, and that the aging process is associated with loss of subcutaneous
fat and increased visceral fat29, i.e., the study population, consisting
solely of young adults, probably has a higher amount of subcutaneous abdominal
fat than visceral fat. Moreover, Pou et al29 called attention to
the fact that, in their study, approximately one quarter of the obese individuals
or with high WC did not have high VAT, while 10% of women and 20% of men with
normal WC had high VAT, suggesting that there are misclassifications between
the categories of clinical adiposity29.

The prevalence
of visceral obesity found in this study was similar to that described by Piernas
Sánchez et al11, who found a prevalence of 28.7% among women.
Pou et al29, when assessing 3,348 participants of the Framingham
Heart Study Offspring and Third Generation Cohort with a mean age of 52.2 ±
9.9 years, found a prevalence of visceral obesity of 44% in females. However,
in addition to the fact that the population was older than that in the present
study, the authors used a cutoff for the classification of different visceral
obesity29 and this may have influenced the high prevalence observed.

In agreement with
the findings of Tadokoro et al10, it was observed that the BMI values
were higher in group with visceral obesity. This finding was also described
by Pou et al29, who observed that the prevalence of VAT increased
with the increasing BMI category.

When comparing
the TG and TC levels between the groups with and without visceral obesity, there
were statistically higher values in the first group only for TG. This finding
can be explained by the fact that, with increasing VAT, free fatty acids are
readily targeted to the liver for further production of glucose, TG, and very-low
density lipoprotein (VLDL)30. Other studies also found higher serum
TG levels in subjects with high VAT4,29,31. However, these studies
found lower levels of HDL in these individuals4,29,31. A limitation
of the present study was the fact that it did not assess cholesterol fractions
(HDL, LDL and VLDL), as the fact that TC was not different between the two groups
may be due to a possible decrease in HDL in the group with visceral obesity.

Tadokoro et al10
and Reyes et al31 did not observe any significant difference regarding
TC values between the two groups.

Regarding blood
pressure, SBP and DBP values were higher in the group with visceral obesity.
However, this finding was not observed in other studies4,10,31,32.
Romero-Corral et al6 draw attention to the fact that the visceral
fat is associated with endothelial dysfunction, even in the absence of blood
pressure alterations. One possible explanation for the increase in BP found
in individuals with visceral obesity is the fact that visceral adipokines and
cytokines may contribute to insulin resistance33. Hyperinsulinemia
can elevate blood pressure through the sympathetic nervous system activation,
the impairment of peripheral vasodilation, an increased response to angiotensin
and increased renal reabsorption of sodium and water, with consequent volume
overload34.

The VVF was positively
correlated with multiple metabolic risk factors in this study (SBP, DBP, TG
and TC). This finding was also observed by other authors32,35. Kotronen
et al32 found a positive and significant correlation between visceral
fat and levels of TG, SBP and DBP (r = 0.36, 0.28 and 0.24, respectively) and
a negative one with HDL (r = -0.38). Hayes et al35 found, in severely
obese women (BMI = 31-67 kg/m2), a significant positive correlation between
intra-abdominal fat and SBP (r = 0.35), DBP (r = 0.31) and a negative one with
HDL (r = -0.34). The correlation with the TG was close to statistical significance
(r = 0.31, p = 0.054)35. Fox et al36, studying individuals
with a mean age of 50 years from the Framingham Heart Study, found a significant
association between SBP (r = 0.30), DBP (r = 0.28), FG (r = 0.34), TG (r = 0.46)
and HDL (r = -0.35) with VAT in women.

In turn, Tadokoro
et al10 found a significant and positive correlation between visceral
fat and SBP and TG only in males, while the TC and DBP showed no significant
correlation with visceral fat in both sexes. It was also observed a negative
correlation between HDL and visceral fat in women, but this study was carried
out with adolescents, with a mean age of approximately 15 years10,
which may have contributed to these findings.

A positive fact
of the present study was that the participants were young adults, allowing the
assessment of the association between fat compartment and cardiovascular risk
factors in the absence of significant comorbidities. Limitations of the study
include two main facts. First, the fact that it did not use imaging methods
to determine the visceral fat (CT, MRI and ultrasonography), due to the high
cost of these methods; however, this equation has been previously validated
to be used in young Brazilian women. Secondly, the study has a cross-sectional
design; thus, the associations are not prospective and causality cannot be inferred.

The prevalence
of visceral obesity found (30.6%) draws attention to the fact that it is a young
female population, which usually has less fat in the visceral region, compared
to older and male individuals. The study also shows that visceral fat was correlated
with age and risk factors for development of CVD (SBP, DBP, TC, TG). The reduction
of visceral fat may therefore contribute to a lower incidence of CVD in later
life. More studies are needed to prospectively evaluate the impact of VAT reduction
on the incidence of risk factors associated with metabolic syndrome and CVD.

Potential Conflict
of Interest

No potential conflict
of interest relevant to this article was reported.

Sources of Funding

This study was
funded by CNPq.

Study Association

This article is
part of the thesis of Doctoral submitted by Marina de Moraes Vasconcelos Petribú,
from Universidade Federal de Pernambuco.